Complex patterns of dopamine‐related gene expression in the ventral tegmental area of male zebra finches relate to dyadic interactions with long‐term female partners

Dopaminergic projections from the ventral tegmental area (VTA) to multiple efferent targets are implicated in pair bonding, yet the role of the VTA in the maintenance of long‐term pair bonds is not well characterized. Complex interactions between numerous neuromodulators modify activity in the VTA, suggesting that individual differences in patterns of gene expression in this region may explain individual differences in long‐term social interactions in bonded pairs. To test this hypothesis we used RNA‐seq to measure expression of over 8000 annotated genes in male zebra finches in established male‐female pairs. Weighted gene co‐expression network analysis identified a gene module that contained numerous dopamine‐related genes with TH found to be the most connected gene of the module. Genes in this module related to male agonistic behaviors as well as bonding‐related behaviors produced by female partners. Unsupervised learning approaches identified two groups of males that differed with respect to expression of numerous genes. Enrichment analyses showed that many dopamine‐related genes and modulators differed between these groups, including dopamine receptors, synthetic and degradative enzymes, the avian dopamine transporter and several GABA‐ and glutamate‐related genes. Many of the bonding‐related behaviors closely associated with VTA gene expression in the two male groups were produced by the male's partner, rather than the male himself. Collectively, results highlight numerous candidate genes in the VTA that can be explored in future studies and raise the possibility that the molecular/genetic organization of the VTA may be strongly shaped by a social partner and/or the strength of the pair bond.     

The effect of solicitations on grooming exchanges among female Japanese macaques at Katsuyama

In group-living primates, individuals often exchange grooming with not only kin but also non-kin. We investigated the effect of soliciting behaviors on grooming exchanges in a free-ranging Japanese macaque (Macaca fuscata) group at Katsuyama. In this study, we used a focal animal sampling method, targeting 14 females. Data were collected for 15.75 ± 2.67 (mean ± SD) hours per focal female. We classified female–female pairs into three pair types: kin pairs, affiliated non-kin pairs, and unaffiliated non-kin pairs. Females received grooming more frequently when they solicited after grooming their partners than when they did not solicit in all pair types. In addition, females received grooming less frequently when they did not groom their unaffiliated non-kin partners before soliciting; prior grooming was not needed to receive grooming from kin or affiliated non-kin partners. The degree of grooming reciprocity did not differ according to the frequency with which females in kin or affiliated non-kin pairs solicited after grooming. On the other hand, grooming reciprocity between unaffiliated non-kin females was more balanced when they solicited frequently after grooming, as compared with when they did not. In conclusion, our study suggests that soliciting behaviors promote grooming exchanges in female Japanese macaques.     

Golden-bellied mangabeys (Cercocebus galeritus chrysogaster) at the Sacramento Zoo: Adult heterosexual pairs

The behaviors of three different adult male–adult female pairs of golden-bellied mangabeys (Cercocebus galeritus chrysogaster) were compared. Correlates of restricted social conditions and of the presence of offspring on adult behavior and direction of aggressive behaviors were noted. A captive pair displayed self-biting and other aberrant behaviors, a lone wild-caught pair showed redirected aggression related to sex, and a pair housed with its offspring showed close social proximity and protection of an infant. The implications of housing and experience for space and visitor exposure are discussed. Observer- vs. visitor-directed displays are seen as important measures of group and visitor effects.     

Correlates and Consequences of the Pair Bond in Steller's Jays

Individuals that maintain pair bonds over multiple breeding attempts are often able to improve reproductive success compared to conspecifics that switch partners. However, the behavioral mechanisms driving this ‘mate familiarity effect’ are still largely unknown. We investigated whether long‐standing pairs in the long‐lived, socially monogamous Steller's jay improved their coordination of movements and behaviors, invested more time in pair bond maintenance, or became more compatible in their tendency to take risks over time compared to newly established pairs. We then compared these pair bond characteristics for successful and unsuccessful partnerships in terms of producing offspring. Jay partners regularly perched together, gave soft contact calls and travelled as a pair even in the non‐breeding season. However, the proportion of observations jay partners spent in each other's company (pair tenacity) was unrelated to risk‐taking behavior of pair members, pair bond duration, or the performance of subtle pair bond maintenance behaviors (i.e., a principle component of behaviors, including soft contact calls, proximity to mates, and frequency of arrival and departure flights with mate). However, evidence suggests that reproductive performance still improved in continuing compared to new pair bonds in Steller's jays. Variation in pair tenacity and frequency of pair bond behaviors may be inconsequential because of jays’ overall high level of contact with partners. Additionally, if jays are able to maximize familiarity early in the pair bond through high overall pair tenacity, the additional benefit of increasing coordination and familiarity with increasing pair bond age may be limited.     

Extra‐pair offspring are less heterozygous than within‐pair offspring in American redstarts Setophaga ruticilla

The vast majority of bird species are socially monogamous; however, extra‐pair paternity is nearly ubiquitous and a number of theories have been proposed to explain the prevalence of this mixed mating strategy. Here, we test the genetic compatibility hypothesis – the idea that females seek extra‐pair copulations with males whose genes are more compatible with her own. For this study, we examined eight years of paternity data (2004–2011) from a Nearctic‐Neotropical migratory bird, the American redstart Setophaga ruticilla, breeding in southeastern Ontario, Canada. We predicted that females paired with genetically similar males (higher relatedness) would be more likely to produce extra‐pair offspring and that extra‐pair offspring would have higher levels of heterozygosity than within‐pair offspring. Alternatively, because this population experiences high levels of immigration, females may produce extra‐pair offspring with more genetically similar males because of the potential for outbreeding depression. Using five highly variable microsatellite markers, we examined patterns of relatedness among social pairs as well as measures of offspring heterozygosity. In contrast to our predictions, we found no difference in relatedness between social pairs where the females produced extra‐pair offspring and social pairs where the females produced only within‐pair offspring. However, extra‐pair offspring were significantly less heterozygous than within‐pair offspring. Together, these findings suggest that females a) are not engaging in extra‐pair fertilizations based on relatedness to their social mate and b) appear to be mating with extra‐pair males that are more genetically similar to themselves. We suggest there may be benefits for females to mate with genetically similar extra‐pair males in highly outbred populations with high rates of immigration, such as for maintaining co‐adapted gene complexes or genes coding for local adaptations.     

Dynamics of Male–Female Multimodal Signaling Behavior across the Estrous Cycle in Giant Pandas (Ailuropoda melanoleuca)

Giant panda courtship behavior includes multimodal signaling assemblages consisting of olfactory, vocal, and postural elements. While signaling is generally conspicuous, successful copulation is inconsistently achieved in captivity, even when female behavioral and physiological data indicate that ovulation is imminent. We set out to characterize these complex patterns of social behavior by observing interactions between 26 unique pairs of giant pandas housed in adjoining pens throughout the females' reproductive cycle. We categorized social behaviors from a transactional perspective and examined social exchanges via analyses of the relative frequency of social behaviors, and via the sequential relationship between male and female social behavior. From non‐estrus to peak‐estrus, we found that the relative frequency of female affiliative and sexual behavior increased and that the relative frequency of ambivalent and aggressive behavior decreased. Male behavior was fairly constant, except for sexual behavior, which increased during peak‐estrus, when it was facilitated by female sexual behavior. Sequential analysis of social interactions showed that preceding behavior had a significant influence over the other panda's response behavior primarily during peak‐estrus, suggesting that pandas are most responsive to conspecific signaling during the peri‐ovulatory period. However, behavioral momentum was a dominant feature of the intra‐individual transitions. Females maintained sexual, ambivalent, and neutral behavior during interactions significantly more than would be expected by chance, with male behavior bearing little influence once the behavior was initiated. A similar pattern was also observed in males, who maintained affiliative, interested, and neutral behaviors. Overall, our data suggest that the multimodal signals used by giant pandas during courtship do not consistently evoke a discrete, immediate response from receivers. Instead, signals appear to advertise reproductive condition and influence potential mates over longer timeframes, suggesting the potential tonic role of communication.     

Behavioral predictors of pairing success in rhesus macaques (Macaca mulatta)

Pair housing is one of the most important components of behavioral management for caged macaques; however, it can result in aggression and injury if partners are incompatible. Knowing when to proceed and when to stop social introductions can be challenging, and can have consequences for the partners. We examined whether behavior early in social introductions predicted success (i.e., partners remained cohoused with full contact for at least 28 days) in 724 female–female and 477 male–male rhesus macaque pairs. We took cage side one–zero focal observations on pairs during the first 2 days of full contact, recording social and aggressive behaviors. The majority of pairs (79.6% of female and 83.0% of male) were successful. The most common behaviors exhibited by pairs during these observations were maintaining proximity, tandem threats, and anxiety. Mounting was also relatively common in male pairs. Grooming and close social contact (e.g., touching) were not common in our study. Several behaviors observed on Day 1 significantly predicted pairing success. For females, these included proximity, tandem threat, rump present, mount, and groom. Day 1 predictors of success for male pairs included proximity, tandem threat, rump present, mount, and social contact. Fewer behaviors predicted success on Day 2. Maintaining proximity on Day 2 predicted success for both sexes, but tandem threat predicted success only for females. Behaviors that predicted incompatibility for females on Day 1 included displace, grimace, threat, bite, and other aggressive contacts. Day 1 predictors of separation for male pairs were displaced, grimace, and abnormal behavior. The only Day 2 behavior that correlated with incompatibility was grimace, which was predictive for males. Interestingly, aggression did not predict incompatibility for male pairs. Identifying behaviors exhibited by monkeys early in the pair introduction that are predictive of long-term compatibility can shape pairing decisions, reducing later stress and potential injury.     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

A positive Link Between Male Testosterone and Spacing Behavior in Pair‐Bonded California Mice

The effects of testosterone (T) on male sexual behavior are well established, but its roles in several associated social behaviors such as pair‐bonding and paternal behavior are diverse. Recently, we reported that male T in response to pairing with a female predicts future paternal behavior in the monogamous and biparental California mouse (Peromyscus californicus). Here, we examined whether T in response to pairing is also associated with spacing behavior between mates under laboratory conditions and if these behavioral patterns are continued during pup care. Pairs of California mice were observed throughout their pair bond before and again after pups were born. We found that males with higher T post‐pairing remained closer to their mates in the weeks before pups were born, and pairs with higher proximity measures during the pair bond spent more time caring for pups together. Overall, these results suggest a similar mechanism for spacing behavior across distinct phases of the pair bond.     

Behavior in adult pairs of captive snow leopards (Panthera uncia)

Eight adult pairs of snow leopards (Panthera uncia) were observed for one to three years in the months December through March to determine the species' social and reproductive characteristics in captivity. To statistically examine the occurrence of behaviors as a function of estrus, the observation weeks were divided into three time blocks: before estrus, estrus, and after estrus. Using percentage of scan samples as an estimate of time spent in various behaviors, 16 behaviors and combined behavior categories were examined for (1) behaviors that differentiated successfully from unsuccessfully breeding pairs, (2) sex differences in behavior, (3) significant correlations between pair members, and (4) behaviors that showed time block effects. The rationale for identifying a behavioral profile of successful breeders in snow leopards was to aid zoos in their captive management programs by increasing their knowledge of the social behavior of this species. By finding correlates to breeding success, informed decisions on whether to change partners after a certain period of time, how to group the cats, and the optimum strategy for a survival plan can be made.     

Identification of selective sweeps in closely related populations of the house mouse based on microsatellite scans

Genome scans of polymorphisms promise to provide insights into the patterns and frequencies of positive selection under natural conditions. The use of microsatellites as markers has the potential to focus on very recent events, since in contrast to SNPs, their high mutation rates should remove signatures of older events. We assess this concept here in a large-scale study. We have analyzed two population pairs of the house mouse, one pair of the subspecies Mus musculus domesticus and the other of M. m. musculus. A total of 915 microsatellite loci chosen to cover the whole genome were assessed in a prescreening procedure, followed by individual typing of candidate loci. Schlötterer's ratio statistics (lnRH) were applied to detect loci with significant deviations from patterns of neutral expectation. For eight loci from each population pair we have determined the size of the potential sweep window and applied a second statistical procedure (linked locus statistics). For the two population pairs, we find five and four significant sweep loci, respectively, with an average estimated window size of 120 kb. On the basis of the analysis of individual allele frequencies, it is possible to identify the most recent sweep, for which we estimate an onset of 400–600 years ago. Given the known population history for the French–German population pair, we infer that the average frequency of selective sweeps in these populations is higher than 1 in 100 generations across the whole genome. We discuss the implications for adaptation processes in natural populations.     

Neighbor effect: evidence of affiliative and agonistic social contagion in captive chimpanzees (Pan troglodytes)

Previous studies of captive chimpanzees have demonstrated the "neighbor effect," or social contagion, with respect to agonistic vocalizations and behaviors. The present study considers whether there is a relationship between behavior patterns in focal animals and the auditory signals of neighboring social groups. Using focal-group sampling, we collected 172.5 hr of data on 51 subjects (25 females and 26 males) housed in 10 social groups. We performed two-tailed Wilcoxon matched-pairs signed-rank tests to determine whether the relative frequency of the vocalizations (high vs. low) affected the behaviors. In keeping with past research, we found that agonistic noises and vocalizations from neighboring social groups had a significant effect on the rates of focal-group bluff displays, pant-hoots, and aggression (P<0.05). In addition, we also found significant relationships between grooming behavior and vocalizations in focal groups, and grooming vocalizations from neighboring groups (P<0.05). The results suggest that social contagion is not limited to aggressive behaviors, but also occurs for affiliative behavior patterns.     

川金丝猴社会行为节目及其动作模式

正确区分和定义川金丝猴各项社会行为节目及其动作模式是研究川金丝猴社会行为的重要基础。本文的目的是按照现代习性学的基本观点,探讨川金丝猴在演化过程中所形成的物种典型行为以及它们的固定动作模式。数据收集时间为1988～2005 年,采用焦点动物取样法和随意取样法,对川金丝猴笼养条件下的繁殖群、半笼养条件下的繁殖群和全雄群、以及其自然栖息地神农架林区的野生猴群进行观察,总计观察约3 000 h。初步确定了川金丝猴54 项物种典型行为节目及其动作模式,其中45 项是群内个体之间用以进行社会交往的社会行为节目,包括8 种在其他灵长类物种中目前还没有报道或比较少见的。     

Species and Hybrid Differences in Frequencies of Play and Agonistic Actions in Canids*

Developmental changes in the frequency of occurrence of some 23 action patterns were studied in pairs of coyotes, wolves, dogs and their hybrids. Over 4,300 entries were recorded from days 24–42 (85.5 h observations in toto). All subjects showed a decrease in contactual behaviors from 24–30 days, and a subsequent increase in play fighting and chasing. In all species, with the exception of the coyotes, the bite was inhibited and play behavior was recorded from 24 days onwards, but only after the 30th day in the coyotes. Species differences in occurrence and frequency of certain action patterns were evident in the wolves, coyotes and dogs, and these differences were also reflected in their hybrids.     

Effects of pair migratory behavior on breeding phenology and success in a partially migratory shorebird population

In migratory systems, variation in individual phenology can arise through differences in individual migratory behaviors, and this may be particularly apparent in partial migrant systems, where migrant and resident individuals are present within the same population. Links between breeding phenology and migratory behavior or success are generally investigated at the individual level. However, for breeding phenology in particular, the migratory behaviors of each member of the pair may need to be considered simultaneously, as breeding phenology will likely be constrained by timing of the pair member that arrives last, and carryover effects on breeding success may vary depending on whether pair members share the same migratory behavior or not. We used tracking of marked individuals and monitoring of breeding success from a partially migrant population of Eurasian oystercatchers (Haematopus ostralegus) breeding in Iceland to test whether (a) breeding phenology varied with pair migratory behavior; (b) within‐pair consistency in timing of laying differed among pair migratory behaviors; and (c) reproductive performance varied with pair migratory behavior, timing of laying, and year. We found that annual variation in timing of laying differed among pair migratory behaviors, with resident pairs being more consistent than migrant and mixed pairs, and migrant/mixed pairs breeding earlier than residents in most years but later in one (unusually cold) year. Pairs that laid early were more likely to replace their clutch after nest loss, had higher productivity and higher fledging success, independent of pair migratory behavior. Our study suggests that the links between individual migratory behavior and reproductive success can vary over time and, to a much lesser extent, with mate migratory behavior and can be mediated by differences in laying dates. Understanding these cascading effects of pair phenology on breeding success is likely to be key to predicting the impact of changing environmental conditions on migratory species.     

The empirical Bayes approach as a tool to identify non-random species associations

A statistical challenge in community ecology is to identify segregated and aggregated pairs of species from a binary presence–absence matrix, which often contains hundreds or thousands of such potential pairs. A similar challenge is found in genomics and proteomics, where the expression of thousands of genes in microarrays must be statistically analyzed. Here we adapt the empirical Bayes method to identify statistically significant species pairs in a binary presence–absence matrix. We evaluated the performance of a simple confidence interval, a sequential Bonferroni test, and two tests based on the mean and the confidence interval of an empirical Bayes method. Observed patterns were compared to patterns generated from null model randomizations that preserved matrix row and column totals. We evaluated these four methods with random matrices and also with random matrices that had been seeded with an additional segregated or aggregated species pair. The Bayes methods and Bonferroni corrections reduced the frequency of false-positive tests (type I error) in random matrices, but did not always correctly identify the non-random pair in a seeded matrix (type II error). All of the methods were vulnerable to identifying spurious secondary associations in the seeded matrices. When applied to a set of 272 published presence–absence matrices, even the most conservative tests indicated a fourfold increase in the frequency of perfectly segregated “checkerboard” species pairs compared to the null expectation, and a greater predominance of segregated versus aggregated species pairs. The tests did not reveal a large number of significant species pairs in the Vanuatu bird matrix, but in the much smaller Galapagos bird matrix they correctly identified a concentration of segregated species pairs in the genus Geospiza. The Bayesian methods provide for increased selectivity in identifying non-random species pairs, but the analyses will be most powerful if investigators can use a priori biological criteria to identify potential sets of interacting species.     

Comprehensive paternity assignment: genotype,spatial location and social status in song sparrows,Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.     

Factors affecting captive whooping crane egg fertility: A retrospective analysis

The whooping crane (Grus americana) has been managed in captivity since the 1960s following a substantial genetic bottleneck in the wild population. Through major ex situ conservation efforts, there are 158 whooping cranes managed in North American institutions and chicks are released annually into the wild. Current reintroduction goals for the whooping crane however, are impeded by poor reproduction within the ex situ population, in part because of low egg fertility. Development of improved management techniques to overcome low egg fertility requires a better understanding of factors that influence egg fertility. We collected data for eggs laid at Patuxent Wildlife Research Center from 2005–2014 (n = 438 eggs; n = 23 pairs). We constructed 5 sets of generalized linear mixed-models, with a Bernoulli-distributed response variable (fertile or infertile), to address the effects of egg-specific variables (month laid, sequence, and clutch order of the egg), life-history events of the male and female (age, rearing method, wing condition, age at first pairing, age at current pairing, and female age at first laying), pair-specific characteristics (kinship, years paired, chick-rearing experience, and previous pairings), and captive management decisions (inclusion in the artificial insemination program and pair experience chick-rearing) on the probability of egg fertility. Our results indicate that female-specific factors (especially age, age at current pairing, and wing status) and pair-specific factors of kinship, chick-rearing experience, copulation, and inclusion in the artificial insemination program influenced fertile egg production. Specifically, the younger a female is when paired with her current social mate, the higher probability that her eggs will be fertile. Furthermore, high kinship reduced fertility, whereas chick-rearing experience and artificial insemination of females with a donor male other than her social mate increased fertility. Further research on mate selection and reproductive mechanisms is needed to better understand egg laying and egg fertility in the whooping crane. © 2019 The Wildlife Society.     

'Multifrequency' location and clustering of sequence patterns from proteins

In previous work, we have shown that a set of characteristics,defined as (code frequency) pairs, can be derived from a proteinfamily by the use of a signal-processing method. This methodenables the location and extraction of sequence patterns bytaking into account each (code frequency) pair individually.In the present paper, we propose to extend this method in orderto detect and visualize patterns by taking into account severalpairs simultaneously. Two ‘multifrequency’ methodsare described. The first one is based on a rewriting of thesequences with new symbols which summarize the frequency information.The second method is based on a clustering of the patterns associatedwith each pair. Both methods lead to the definition of significantconsensus sequences. Some results obtained with calcium-bindingproteins and serine proteases are also discussed. Received on March 6, 1990; accepted on September 24, 1990